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Trophic Transmission, Distribution and Host-Specificity in Hedruris Spinigera (Nematoda: Hedruridae)

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Trophic Transmission, Distribution and Host-Specificity in Hedruris Spinigera (Nematoda: Hedruridae) FOLIA PARASITOLOGICA 57[3]: 223–231, 2010 © Institute of Parasitology, Biology Centre ASCR ISSN 0015-5683 (print), ISSN 1803-6465 (online) http://www.paru.cas.cz/folia/ New evidence on a cold case: trophic transmission, distribution and host-specificity in Hedruris spinigera (Nematoda: Hedruridae) José L. Luque1, Fabiano M. Vieira2, Kristin Herrmann3, Tania M. King3, Robert Poulin3 and Clément Lagrue4 1 Departamento de Parasitologia Animal, Universidade Federal Rural do Rio de Janeiro, Caixa Postal 74.508, CEP 23851-970 Seropédica, RJ, Brasil; 2 Curso de Pós-Graduação em Biologia Animal, Universidade Federal Rural do Rio de Janeiro, Seropédica, RJ, Brasil; 3 Department of Zoology, University of Otago, P.O. Box 56, Dunedin 9054, New Zealand; 4 Laboratoire d’Ecologie Fonctionnelle (EcoLab, CNRS UMR 5245), 29 Rue Jeanne Marvig, BP 24349, 31055 Toulouse cedex 4, France Abstract: The life cycle of Hedruris spinigera Baylis, 1931 (Nematoda: Hedruridae) is determined here with the first formal iden- tification of the parasite’s intermediate host: the crustacean amphipod Paracorophium excavatum Thomson. Adult H. spinigera are redescribed from specimens collected from the stomach of fishes, Retropinna retropinna (Richardson) and Aldrichetta forsteri (Va- lenciennes), from Lake Waihola, New Zealand. Immature adults of the parasite collected from intermediate hosts (P. excavatum) are also described for the first time. The prevalence, abundance and intensity of infection ofH. spinigera in several fish species are quan- tified along with the occurrence of P. excavatum, the parasite’s intermediate host, in fish stomach contents. Although H. spinigera’s transmission mode (trophic transmission) and fish diet potentially expose all fish species to infection, some level of host specificity must exist as parasite prevalence, abundance and intensity of infection vary greatly between potential definitive host species. We sug- gest here that the anatomy of the fish digestive tract and especially that of the stomach plays an important role in host suitability for H. spinigera. While P. excavatum is the only intermediate host in Lake Waihola, H. spinigera was found in six different fish species: Aldrichetta forsteri, Galaxias maculatus (Jenyns), Retropinna retropinna, Rhombosolea retiaria Hutton, Perca fluviatilis Linnaeus and Salmo trutta Linnaeus; although typical hedrurid attachment and mating positions were observed only in R. retropinna and A. forsteri. The limited distribution of H. spinigera is most likely due to that of its different host species (intermediate and definitive), all inhabitants of coastal fresh and brackish waters. Keywords: Hedruris spinigera, nematode, host specificity, parasite distribution, amphipod, fish Hedruris Nitzsch, 1821, the only genus of the family 1989, Bursey and Goldberg 2000, 2007). Currently, the Hedruridae (Nematoda), consists of parasites of the di- development cycles of only three species have been in- gestive tracts of fishes, frogs, salamanders, lizards, and vestigated: H. androphora Nitzsch, 1821, H. ijimai Mor- turtles. Hedruris was first proposed by Nitzsch (1821) ishita, 1926 and H. suttonae Brugni et Viozzi, 2010 (Pet- to include Hedruris androphora from intestine of Tritu- ter 1971, Hasegawa and Otsuru 1979, Brugni and Viozzi rus cristatus (Laurenti) (Caudata, Salamandridae). Until 2010). recently and the description of a new species from Ar- In New Zealand, there have been very few studies of gentina (Brugni and Viozzi 2010), there were 22 docu- larval nematodes, and nematode development cycles are mented nominal species of Hedruris distributed world- seldom described (Moravec et al. 2003). For example, wide (Bursey and Goldberg 2000, 2007). As common Hedruris spinigera Baylis, 1931 is a common freshwater characters, Hedruris species possess four complex lips, parasite typically found in the stomach of fish where the oesophagus���������������������������������������������� not clearly divided into muscular and glandu- larger female attaches itself deeply into the stomach epi- lar portions, and the terminal end of the female is modi- thelium using a recurved hook in its tail (Fig. 1A, Clark fied into an attachment or prehensile organ (Petter 1971, 1978, McDowall 1990). The smaller male lacks the at- Hasegawa and Otsuru 1979, Anderson 2000). Species of tachment structure and moves freely in the stomach lu- Hedruris are distinguished on the basis of the number and men until it finds a female already attached to the host arrangement of caudal papillae in the male, appearance of and curls around her body (Fig. 1B, Clark 1978, Jellyman eggs in females and morphology of cephalic structures, 1989). Taxonomically, Hedruris spinigera is most similar spicules and female caudal hook (Baker 1986, Hasegawa to H. bryttosi Yamaguti, 1935, H. miyakoensis Hasegawa, Address for correspondence: C. Lagrue, Laboratoire d’Ecologie Fonctionnelle (EcoLab, CNRS UMR 5245), 29 Rue Jeanne Marvig, BP 24349, 31055 Toulouse cedex 4, France. Phone: +33 (0)5 62 26 99 65; Fax: +33 (0)5 62 26 99 99; E-mail: [email protected] 223 lies in the consideration of fish diet and the identification of the intermediate host(s). During recent investigations into the parasites of freshwater fish in southern New Zea- land, adult H. spinigera were observed in the digestive tract of several fish species, and infections were linked to the consumption of a common brackish water crustacean, the amphipod Paracorophium excavatum Thomson. Pre- viously, Luque et al. (2007) described parasitic nematode larvae from P. excavatum from the same location and clas- sified these asHysterothylacium sp.; here, we critically re- examine this identification in the light of morphological and molecular data on adult H. spinigera. The nematode’s sexually mature adults from definitive hosts and imma- ture adults (i.e. larval stages) from intermediate hosts are matched formally for the first time using molecular evidence and described morphologically; further, the life cycle is determined and host specificity of the parasite is discussed from the results on fish diet and H. spinigera prevalence and abundance in the different fish species. MATERIALS AND METHODS The parasites were found in several samples of the amphipod Paracorophium excavatum and different fish species collected from the same location. Samples were taken between November Fig. 1. Hedruris spinigera Baylis, 1931, light microscopy of 2008 and February 2009 (Austral summer) along a short stretch mature adults from fish definitive hosts. A – large female with of the shore of Lake Waihola (46°01′S, 170°05′E), near Dun- tail end anchored about two-third through the fish host stom- edin, South Island, New Zealand. Lake Waihola is a shallow, ach epithelium, smaller males in the background; B – mature coastal lake situated 10 km from the Pacific Ocean and influ- male and female shown in typical attachment position with male coiled around tail end of female. Specimens were still attached enced twice daily by a fresh to brackish tidal input, depending to fish stomach epithelium when fixed in 70% ethanol. on tides and river flow (Hall and Burns 2002). Only one other amphipod species is present in Lake Waihola, Paracalliope fluviatilis Thomson. However, despite extensive sampling, no 1989 and H. hanleyae Bursey et Goldberg, 2000 with H. spinigera infection was ever found in this species (Lagrue males exhibiting 10 pairs of papillae and females produc- and Poulin 2008a, b). It is also important to note that although ing nonmammillated eggs. Nevertheless, H. spinigera has Hedruris species occur commonly in amphibians (Chandler one pair of precloacal papillae and one pair of adcloa- 1919, Hasegawa and Otsuru 1979, Anderson 2000, Bursey and cal papillae while H. bryttosi lacks precloacal papillae Goldberg 2000), these potential definitive hosts are totally absent (Yamaguti 1935). Similarly to H. spinigera, H. miyakoen- from Lake Waihola. New Zealand amphibian fauna is naturally sis has one (or two) pair of precloacal papillae (Hasegawa very poor and comprises only few species of highly specialized 1989) but the spicules and the anterior end are morpho- and geographically restricted frogs of the genus Leiopelma (Bell 1978, Towns and Daugherty 1994). logically different from those of H. spinigera. Finally, Nine samples of 150 P. excavatum (1350 individuals in total) H. hanleyae has two pairs of precloacal papillae (Bursey were collected at regular intervals during the sampling period. and Goldberg 2000). Amphipods were captured using a push-net (500 µm mesh size) Intriguingly, although H. spinigera is widely distrib- and dredging the surficial sediment whereP. excavatum burrows. uted within New Zealand and can infect a variety of fish, The retained sediment with associated organisms was placed in this parasite occurs only near coastal areas, especially sorting trays from which P. excavatum individuals were collect- in brackish waters (Stokell 1936, Hine 1978, Jellyman ed (Schnabel et al. 2000). Amphipods were kept alive in plastic 1989). No satisfactory explanation has ever been pro- containers filled with local water and brought back to the labora- posed for this geographical restriction although fish diet tory for later dissection. Fish were collected weekly during the and the identity of intermediate host species have been sampling period using gillnets constructed by Oy Lindeman Ab hypothesized to determine the distribution and abundance of Finland and a standard purse seine net. For gillnetting, three 25
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